REVIEW

Imaging-guided chest biopsies: techniques and clinical results

Michele Anzidei1 & Andrea Porfiri1 & Fabrizio Andrani1 & Michele Di Martino1 &

Luca Saba2 & Carlo Catalano1 & Mario Bezzi1

Received: 22 December 2016 /Revised: 7 May 2017 /Accepted: 18 May 2017 /Published online: 21 June 2017# The Author(s) 2017. This article is an open access publication

AbstractBackground This article aims to comprehensively describeindications, contraindications, technical aspects, diagnosticaccuracy and complications of percutaneous lung biopsy.Methods Imaging-guided biopsy currently represents one ofthe predominant methods for obtaining tissue specimens inpatients with lung nodules; in many cases treatment protocolsare based on histological information; thus, biopsy is frequent-ly performed, when technically feasible, or in case other tech-niques (such as bronchoscopy with lavage) are inconclusive.Results Although a coaxial system is suitable in any case, twocategories of needles can be used: fine-needle aspiration biop-sy (FNAB) and core-needle biopsy (CNB), with the latterdemonstrated to have a slightly higher overall sensitivity,specificity and accuracy.Conclusion Percutaneous lung biopsy is a safe procedureeven though a few complications are possible: pneumothorax,pulmonary haemorrhage and haemoptysis are common com-plications, while air embolism and seeding are rare, but poten-tially fatal complications.Teaching points• Imaging-guided biopsy is one of the main methods to obtainlung nodule specimens.

• CT has the highest accuracy for diagnosis as an imagingguide.

• Compared to FNAB, CNB has a higher accuracy fordiagnosis.

• Pneumothorax and parenchymal pulmonary haemorrhagecare the most frequent complications.

• Several clinical and technical variables can affect diagnos-tic accuracy and patient safety.

Keywords Lung lesion . Percutaneous biopsy .

Complication . Diagnostic accuracy . Fine-needle aspirationbiopsy (FNAB) . Core-needle biopsy (CNB)

Introduction

Chest tumours, in particular lung cancer, remain one of themost common causes of cancer-related death worldwide.Withthe diffusion of spiral CT, an increasing number of lung andmediastinal lesions is detected and histological diagnosis isoften necessary to determine the most appropriate manage-ment of these lesions [1]. In this clinical scenario, imaging-guided biopsy is one of the main methods to obtain tissuespecimens. Various imaging techniques including computedtomography (CT) fluoroscopy and ultrasound (US) can beused to guide chest biopsies, but CT is most frequentlyemployed because of its high spatial and contrast resolutionas well as its 3D imaging ability; in many cases CT ispreferred based on the localisation of the nodule orother patient-related factors.

Clinical indication

Clinical indications of imaging-guided chest biopsy have sig-nificantly changed from the introduction of the technique as aresult of technical advances in needle technology, imaging

* Michele Anzideimichele.anzidei@uniroma1.it

1 Department of Radiological, Oncological and AnatomopathologicalSciences, Radiology, Sapienza, University of Rome, PoliclinicoUmberto I, Viale Regina Elena, 324, 00161 Rome, Italy

2 Department of Radiology, Azienda Ospedaliero Universitaria(A.O.U.), di Cagliari, Polo di Monserrato, Italy

Insights Imaging (2017) 8:419–428DOI 10.1007/s13244-017-0561-6

modalities, pathological analysis and immunohistochemistrytechniques. The introduction of PET-CT further modifiedthese indications, reducing the percentage of unnecessary bi-opsies [2]. At present, the growing list of indications (Table 1)includes histological diagnosis of undetermined and otherwisenot characterisable pulmonary, mediastinal and chest wall le-sions as well as biopsy or re-biopsy of known malignant le-sions to obtain histological material for targeted therapy.(Fig. 1).

A new or enlarging solitary nodule or mass

The increasing clinical use of chest CT has resulted in anincreasing incidental detection of small pulmonary nodules.In particular, pulmonary nodules are incidentally detected inaround 8.5% of the general population [3] and in up to 51% ofsubjects with risk factors [4]. Therefore, a new or enlargingsolitary nodule is the most common indication for imaging-guided chest biopsy. If a nodule is initially identified at con-ventional chest radiography, CT investigation is necessary tocharacterise the lesion, estimate the likelihood of malignancy[5] and identify lymphadenopathies or other accessible sitesfor biopsy (such as extra-thoracic metastases) [6, 7]. PET-CTexamination may also be helpful in the management of pul-monary nodules larger than 1 cm, reducing the need of punc-ture of non-enhancing solid nodules [4–8] and with a sensi-tivity of 94% and a specificity of 83% for solid pulmonarynodules between 1 and 3 cm in diameter [9]. It must betaken in consideration that active inflammation (i.e. ac-tive tuberculosis, histoplasmosis, rheumatoid nodules)may cause false positives on PET-CT scans because oftheir high glucose metabolism [10]. On the other hand,low-grade malignant tumours, such as carcinoid [11] orlow-grade adenocarcinoma [12], may produce false-negative results because of their low glucose metabo-lism. In these cases, careful follow-up with CT mustbe performed according to well-established guidelinesto demonstrate regression/disappearance of the noduleafter therapy or to address patients to biopsy if persis-tence or increase in size are evident [13].

Multiple nodules in a patient without known neoplasticdisease or in prolonged remission

Several benign conditions can appear with slowly enlarging ormultiple new pulmonary nodules, such as rheumatoid arthritis,sarcoidosis or infectious diseases, including tuberculosis andfungal infections, particularly in immunosuppressed patients[14–16]. In these cases appropriate clinical work-up and CTfollow-up are sufficient to exclude malignancy. Neverthelessmultiple nodular lesions may be the initial metastatic presen-tation in a patient with an unknown primary tumour or the signof disease progression in a patient with known primary

tumour in prolonged remission. In these cases imaging-guided biopsy may be necessary to confirm or excludemalignancy.

Focal parenchymal infiltrates in which an infectiousorganism cannot be isolated

When infectious organisms cannot be isolated from theculture of sputum, blood or lung lavage, lung biopsycan be necessary to obtain tissue samples for patholog-ical examination. The biopsy sample can be cultured fordiagnostic purposes to establish the most appropriatepharmacological treatment. Imaging-guided biopsy wasdemonstrated to have a sensitivity of 80% and a posi-tive predictive value of 100% [17, 18].

Diagnosis of hilarmasses following negative bronchoscopy

Transbronchial needle aspiration during bronchoscopy or un-der ultrasound guidance is still considered the reference tech-nique for the diagnosis of hilar masses [19, 20]. However,when bronchoscopy cannot be performed or is inconclusive,hilar masses can be accurately diagnosed by imaging-guidedbiopsy.

Undiagnosed mediastinal mass

Mediastinal masses are most frequently located in the anteriormediastinum and include a variety of different entities, such asthymic malignancy, lymphomas, endocrine tumours and ma-lignant germ cell tumours [21]. In the absence of typical clin-ical and imaging features, histological diagnosis is necessary[22]; imaging-guided biopsy should be always attemptedin accessible lesions before diagnostic mediastinoscopyor in case of inconclusive results of mediastinoscopy.

Biopsy or re-biopsy of malignancy for targeted therapy

Advanced non-small-cell lung cancer in progression afterfirst-line therapymay need imaging-guided re-biopsy to detect

Table 1 Indications for imaging-guided chest biopsy

Indications for imaging-guided chest biopsy

1. A new or enlarging solitary nodule or mass

2. Multiple nodules in a patient without known neoplastic disease or inprolonged remission

3. Focal parechymal infiltrates in which an infectious organism cannot beisolated

4. Diagnosis of hilar masses following negative broncoscopy

5. Undiagnosed mediastinal mass.

6. Bipopsy or re-biopsy of malignancy for targeted therapy.

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a possible new biological profile and to guide therapeuticdecision-making in more than one-third of cases. [23].

Contraindications

Because of moderate risk of bleeding, abnormal clotting func-tion or thrombocytopenia should be recognised and correctedbefore the procedure. Thus, oral anticoagulants andantiaggregant drugs should be reduced or stopped to reachan international normalised ratio (INR) of less than 1.5 andan activated partial thromboplastin time (aPTT) not more than1.5 times the control value; platelet transfusion is recommend-ed for counts <50,000/μl (Table 2) [24]. Suspected hydatidcyst or arterio-venous malformation should not be biopsiedbut can be identified on CT. Mechanical ventilation, whichmay lead to pneumothorax and favours air embolism, inabilityof a patient to co-operate during the procedure or to suspendrespiration on request or control cough are the major contra-indications. A unique functional lung is often considered an-other contraindication, while severe chronic obstructive pul-monary disease, pulmonary hypertension or cardiac insuffi-ciency do not constitute absolute contraindications but in-crease the complication rate. [25].

Imaging guidance techniques

CT, fluoroscopy and US may all be used to guide chest biop-sies and operators should be familiar with the advantage andlimitations of each one [26]. Parameters affecting the selectionof the most appropriate imaging technique are lesions site, sizeand visibility as well as its relationship with critical anatomicalstructures to be avoided [5]. Whenever possible, chest biop-sies should be performed under US guidance (Fig. 2) to ex-ploit the advantages of real-time monitoring without radiationexposure to patients and operators [27]; however, US guid-ance is limited to superficial lesions adjacent to the chest walland/or to lesions delineated by pleural effusion sufficient to

Table 2 Abnormal values that should be corrected before the procedure

Patient management before procedures with moderate risk of bleeding

INR Correct to <1.5

aPTT Should be corrected for values >1.5 × control

Plateles Transfusion recommended for count <50.000/μl

Fig. 1 Indications for CT-guidedchest biopsy. (a) Solitarypulmonary nodule. (b)Parenchymal infiltrates in whichan infectious organism cannot beisolated. (c) Hilar mass followingnegative bronchoscopy. (d)Undiagnosed mediastinal mass

Fig. 2 Ultrasound-guided chest biopsy of a pulmonary nodule in theright lower lobe

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create a suitable interface for ultrasound penetration. In thevast majority of cases, CT (or cone-beam CT) (Figs. 3 and4) is the preferred guidance method for chest biopsies due toits optimal spatial and contrast resolution as well as its 3Dimaging ability. Furthermore an intravenous contrast agentcan be used to differentiate target lesions from atelectasis,necrosis and vascular structures. CT-guided chest biopsiescan be performed either with the step-and-shoot approach orwith CT-fluoroscopy (Fig. 5): while the step-and-shoot ap-proach allows 3Dmultiplanar reconstruction and significantlyreduces the radiation dose to the patient and operators, it doesnot allow real-time monitoring of lesion movement duringrespiration and is strongly influenced by the patient compli-ance. On the other hand, real-time monitoring of lesionsmovement with CT-fluoroscopy guidance allows reducingneedle passes and procedure time; however, the radiation dose(to both the patients and operator) is significant [28]. To sim-plify the approach and to increase the speed and reliability ofstep-and-shoot CT-guided chest biopsies, several technical ad-vances have been proposed, including augmented reality anduse of robotic platforms [29].

Furthermore, if a PET/CT is available, the needle should beled to the most enhancing area of the lesion to increase diag-nostic accuracy.

Biopsy procedure

Patient positioning and instruction

The patient should be positioned prone, supine or lying on theside, based on the previously planned access site and needletrajectory. When needed, arms can be raised above the head towiden the intercostal spaces and obtain easier access. Theprocedure should be adequately explained to the patients withemphasis on the potential stinging sensation during the pleuralpuncture and breath-hold phases.

Access site

Whenever possible, the needle access site should be cephalicto the ribs to avoid intercostal vessel and nerves puncture(Fig. 6) [30]. In case of anterior parasternal access, inter-nal mammary vessels should be carefully avoided [31].Costal cartilage may traversed if needed but this mayresult in reduced needle mobility. The skin in the accesssite should be sterilised with standardised antiseptic so-lution and cutaneous and subcutaneous tissues should beinfiltrated with lidocaine (lignocaine) up to a maximumdose of 20 ml of a 2% solution.

Fig. 3 CT-guided chest biopsy ofa pulmonary nodule in the leftlower lobe. (a) Axial, (b) coronaland (c) sagittal intraproceduralCT scans showing the needle tipin the lesion (arrow)

Fig. 4 Axial images during fluoroscopy-guided chest biopsy of a solitary subpleural nodule

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Breath-hold techniques and needle manipulation

The breath-hold technique stabilises the positions of the dia-phragm, pleural planes, lung, fissures and, ultimately, targetlesions; however, breath-hold capabilities can be extremelydifferent from patient to patient, and even the same subjectmay not be able to reproduce breath-hold during the procedurebecause of stress or fatigue. Therefore, it can be easier to targetlarger tumours (>2/3 cm) instructing the patient to breath free-ly with shallow respiration; even though the target lesionsmoves slightly, its large size may be sufficient to require fewadjustments. In the remaining cases, the patient can beinstructed to maintain an inspiratory or expiratory apnoea toallow easier access to target lesions.

Needle types

Needle choice is based on the size and location of the lesion,intended needle trajectory, information expected from thepathologic sample, status of the lung parenchyma and operator

preference. Some of the more commonly used fine-needleaspiration (FNA) devices include Chiba, Franseen, Westcott,MaxiCELL, Greene (Cook) and Turner (Cook) needles,which have circumferentially sharpened tips allowing for sam-pling. Core biopsy needles are designed to collect a smallpiece of tissue intended for surgical pathology analysis andcan be designed as end-cutting or side-cutting devices. Themost commonly used core biopsy needle is the Tru-Cut, whichconsists of an outer cutting cannula and an inner slotted stylet.The Temno core biopsy device is another similar commonlyused automatic core biopsy needle. The Biopince full core isan automated end-cutting needle that produces a full cylindri-cal core specimen. The decision to perform core biopsy orboth core biopsy and FNA is multifactorial and highly insti-tution-/operator-dependent [28]. The number of passes neededper procedure has not been defined, but the decision to per-form more than one puncture depends on procedure difficulty,risk of complications, quality of the first specimen obtainedand the pathologist’s requests. The presence of an on-site pa-thologist may reduce the number of biopsies needed [5]. Also

Fig. 5 Progressive images of Cone-beam-guided chest biopsy of a pulmonary nodule in the left upper lobe

Fig. 6 (a) Axial CT image and(b) 3D reconstruction showinginternal mammary arteries(arrows), which must be avoidedduring the procedure

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the use of a coaxial, a larger-bore needle that is kept in place tomaintain access to the target lesion, may allow multiple tissuesampling, reducing repeated pleural or soft tissue punctures[32]. Several techniques have been proposed to seal the pathof the needle after its removal to reduce the risk of pneumo-thorax and haemorrhage; the most successful option is to cre-ate a blood patch with autologous venous blood [33, 34].

Diagnostic accuracy

Ultrasound versus CT

In a recent meta-analysis, Di Bardino et al. compared the diag-nostic accuracy of ultrasound and CT-guided thoracic biopsy.The overall pooled diagnostic accuracy of ultrasound-guidedbiopsy was 88.7% (446/503), with a sensitivity of 91.5% (366/400) and a specificity of around 100% for the diagnosis ofmalignancy. The overall pooled diagnostic accuracy of CT-guided biopsy was 92.1% (9567/10,383), with a sensitivity of92.1% (7343/7975) and a specificity of around 100% for thediagnosis of malignancy (Tables 3 and 4) [35]. These data showa relative superiority of CT as guidance method, but data onCT-guided biopsies weremore significant because of the highernumber of cases in comparison with US-guided biopsies.

FNAB versus core biopsy

There is a wide variation in reporting diagnostic accuracies offine-needle aspiration biopsy (FNAB) between different insti-tutions, ranging from 64% to 97%. The false-negative rate ofFNAB varies, occurring in 6 to 54% of biopsies. The sensi-tivity, specificity and accuracy of FNAB for pulmonary le-sions are 82 to 99%, 86 to 100% and 64 to 97%, respectively[28]. Core biopsy has been shown to have slightly higheroverall sensitivity, specificity and accuracy, with respectivevalues of 89%, 97% and 93% (Table 3). Several recent papersadvocate the use of 18- and 20-gauge cutting needles as wellas coaxial techniques to improve the diagnostic yield,reporting diagnostic accuracies of 74–95% for the diagnosisof malignancy. Charig and Phillips reported similar accuracyof FNAB and core biopsy when an on-site pathologist wasavailable; in a similar setting Capalbo et al. observed a greater

diagnostic accuracy of FNAB compared to core needle biopsy(94.83% vs. 81.82. %) [36]. Nowadays, the test of geneticmutations is important to plan targeted therapies in patientwith lung cancers. With regard to this point, Schneider et al.observed a statistically significantly higher number of samplessufficient for molecular testing in core biopsy than FNAB(67% vs. 46%; P = 0.007) [37].

Central versus peripheral lesions

Various studies evaluated the effects of lesion location on thediagnostic accuracy of imaging-guided biopsy in chest tu-mours. In a paper from Layfield et al. [38], the sensitivity indiagnosing lung tumours decreased from 100% in peripherallesions to 82% in central lesions; however, this study wasconducted in 1996 with basic CT equipment, as demonstratedby the striking differences in sensitivity between fluoroscopyguidance (97%) and CT guidance (80%). Yamagamy et al.[39] demonstrated that some peripherally located lesions arenot accessible at all with conventional CT guidance because oftheir relationship with rib arcs, thus requiring needle position-ing under CT-fluoroscopy guidance. Finally, Wang et al. [40]recently compared the rates of complications and diagnosticaccuracy of CT-guided biopsy in peripheral versusparamediastinal lesions, demonstrating how this techniquemay be safe and reliable even for deeply located tumours; inparticular, their paper reports diagnostic accuracy of 95.4% inparamediastinal lesions and 94.7% in peripheral lesions, witha sensitivity of 95.6% and 94.2% respectively (Table 3).

Post-procedural care and complications

Once the biopsy has been performed, a CT scan of the chest isobtained to identify any immediate post-procedural

Table 3 Test characteristics fordifferent imaging guidancetechniques (ultrasound vs. CT),biopsy techniques (FNAB vs.core biopsy) and lesion location(pamediastinal vs. peripheral)

Accuracy Sensitivity Specificity

Imaging guidance techniqueE Ultrasound-guide biopsy 88.7% 91.5% 100%

CT-guide biopsy 92.1% 92.1% 100%

Biopsy technique FNAB 64–97% 82–99% 86–100%

Core biopsy 93% 89% 97%

Lesion location Paramediastinal 95.4% 95.6% 100%

Peripheral 94.7% 94.2% 100%

Table 4 Safety profile of imaging-guided biopsy

PTX Haemorrhage

CT-guided biopsy 20.5% 2.8%

Ultrasound-guided biopsy 4.4% –

Fluoroscopy-guided biopsy 11.1% –

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complications. According to some authors, the patients shouldbe rolled over onto the punctured side to reduce the risk ofdelayed PNX; anyway, this is a controversial opinion, sinceother authors have reported no benefits of putting patients inthe Bbiopsy down position^ [41]. Following measures includeobservation andmonitoring of vital signs for at least 4 h. Chestfilms are usually acquired after 4 h to detect possible asymp-tomatic PNX. If the clinical suspicion of a PNX arises, chestradiography must be obtained immediately. In low-risk pa-tients, many interventional radiology services reasonably per-form lung biopsies on an outpatient basis, with discharge at4 h and readmission only if symptoms develop [42].

Pneumothorax

PNX is the most common complication after imaging-guidedchest biopsy; it is most frequently detected after lung biopsybut can also occur even after biopsies of mediastinal, pleuraland chest wall lesions. Usually PNX occurs during or imme-diately after the procedure and it is detected on post-procedural control scans. The incidence of PNX has beenreported to be up to 61% with an average risk of 20%[43–46]. Risk factors for PNX can be related to patient orlesions features, but also to the biopsy technique. In particular,the rate of PNX increases with the patient age and severity ofunderlying lung disease (e.g. emphysema or chronic obstruc-tive disease) [47, 48] as well as in smaller and deeper lesions[49, 50]. Technical risk factors include the type and size ofbiopsy needle, longer procedure duration, biopsies in the mid-dle or lower lobe, transgression of a fissure and multiple nee-dle repositioning or pleural passes [51]. A PNX developedduring the procedure can be immediately aspirated throughthe introducer needle or a separate needle inserted into thepleural space, preventing further enlargement; however someauthors suggest placing a chest tube if aspirated air is greaterthan 670 ml [40]. PNXs developed after the procedure (Fig. 7)are often small and asymptomatic and can be managed con-servatively by monitoring vital signs and performing serialchest films (at 1 and 4 h) [45, 52]. Nevertheless, in a minority

of cases (1–14%), PNX can be significant (>30% of lungvolume), increase over time or become symptomatic. In thesecases small-calibre, 6- to 9-French catheters can be safely andeasily placed under CT guidance [41, 53, 54].

Pulmonary haemorrhage and haemoptysis

Pulmonary haemorrhage represents the second most commoncomplication after imaging-guided biopsy. PHmay occur withor without haemoptysis and can be easily detected on screen-ing post-biopsy CT scan as a perilesional or needle tractground-glass opacity (Fig. 8). The occurrence rates of PHare estimated to be from 4 to 27% (with an average incidenceof 11%), while haemoptysis risk is up to 5% [55, 56]. Usuallythis complication does not need any treatment and the onlyrecommendations is to place the patient in a lateral position,with the biopsy side down, to avoid aspiration of blood intothe unaffected lung [44]. Occasionally a larger, higher-gradePH occurs and oxygen as well as pro-coagulative therapy maybe needed. Risk factors for higher-grade PH include older age,female sex, emphysema, pulmonary hypertension, coaxialtechnique, subsolid lesions, nonsubpleural location and lesionsize smaller than 3 cm [57, 58]. Avoiding PH is important tomanage patients with abnormal coagulation profiles and tocorrect the diathesis before the procedure. In such pa-tients, more invasive biopsy techniques that imply theuse of the core needle and coaxial technique should beavoided as should prolonged procedures with extendedneedle paths [45, 59]. Finally, haemothorax is an ex-tremely rare and more severe complication, usually dueto puncture of an intercostal or less commonly a largethoracic vessel, or mammary vessels in the case of ananterior parasternal biopsy.

Air embolism

The occurrence of systemic air embolism (SAE) in the leftatrium, left ventricle or systemic circulation is a rare (inci-dences between 0.01% and 0.21%), but potentially fatal (by

Fig. 7 CT-guided chest biopsy ofsolitary pulmonary nodule in theleft lower lobe. (a) Axial CTimage before the procedureshowing the subpleural nodule.(b) Post-procedural axial CTimage showing small PNX(arrows) as a complication oftransthoracic biopsy

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brain or cardiac infarct) event [59] (Fig. 9). There are threemechanisms in particular responsible for SAE during biopsy:placement of the needle tip in a pulmonary vein, formation ofa bronchial-venous or alveolar-venous fistula and opening theouter cannula of a coaxial biopsy needle to the atmosphere.Risk factors can be biopsy of cystic or cavitary lesions (i.e.vasculitic granulomas), coughing during the biopsy and pos-itive pressure ventilation [60]. In a study from Freund et al.,asymptomatic SAE detectable at CT after lung biopsy wasreported to be as high as 3.8% (23/610 patients), whereasthe symptomatic cases were 0.49%. In the meta-analysis fromTomiyama et al. [61, 62], the incidence of SAE ranges from0.001% to 0.003%, being influenced by the depth of needlepenetration into the lesion, endotracheal anaesthesia, locationof the lesion above the level of the left atrium and proneposition of the patients [61].

Tumour seeding

Tumour seeding through the needle tract represents a very rarecomplication with a prevalence reported in the literature be-tween 0.012 and 0.061% [45]. The real clinical relevance isstill discussed, but it is obvious that tumour seedingalong the needle tract can significantly change patient

management and life expectancy and should be strictlyavoided [63]. Tumour seeding is reported to be morefrequently observed after imaging-guided core needlebiopsy of pleural mesothelioma [64].

Complications by imaging guidance technique

In the meta-analysis from Di Bardino et al. US-guidedbiopsy was generally very well tolerated and safe, witha pooled incidence of PNX of 4.4% (22/503) in thereported papers. This looks favourable compared toCT-guided biopsy, but is also obviously correlated to astatistical bias in lesion position since the targets of US-guided biopsies are usually adjacent to or infiltrating thepleural surface, with a very low risk of PNX.

Compared with the conventional step-and-shoot approachfor CT-guided biopsy, CT fluoroscopy is faster and requiresfewer needle passes, resulting in a decrease of procedure du-ration and fewer complications. In particular Heck et al. [48]showed a trend toward a lower PNX rate when usingCT fluoroscopy as guidance method. Similar resultshave been obtained by Kim et al. [65], with a decreasefrom 27.1% to 11.1% in PNX rates when using CTfluoroscopy.

Fig. 9 Post-procedural CT scanafter chest biopsy showing twodifferent patients with airembolism in cerebral vessels(arrows)

Fig. 8 CT-guided chest biopsy ofa pulmonary nodule. (a) Axial CTimage before the procedureshowing a pulmonary nodule inthe right lower lobe. (b) Post-procedural axial CT imagedemonstrates perilesionalhaemorrhage as ground-glassopacity around the nodule(arrows)

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Conclusions

In conclusion, imaging-guided chest biopsy is an intervention-al procedure of pivotal importance for several clinical condi-tions of pneumological, oncological and surgical interest. Thisprocedure may appear very simple and linear, but radiologistsapproaching it for the first time must consider several clinicaland technical variables significantly affecting the final results,in terms of both diagnostic accuracy and patients’ safety.

Open Access This article is distributed under the terms of the CreativeCommons At t r ibut ion 4 .0 In te rna t ional License (h t tp : / /creativecommons.org/licenses/by/4.0/), which permits unrestricted use,distribution, and reproduction in any medium, provided you give appro-priate credit to the original author(s) and the source, provide a link to theCreative Commons license, and indicate if changes were made.

References

1. Viggiano RW, Swensen SJ, Rosenow EC 3rd (1992) Evaluationand management of solitary and multiple pulmonary nodules.Clin Chest Med 13(1):83–95

2. Nomori H, Watanabe K, Ohtsuka T, Naruke T, Suemasu K, Uno K(2004) Evaluation of F-18 fluorodeoxyglucose (FDG) PET scan-ning for pulmonary nodules less than 3 cm in diameter, with specialreference to the CT images. Lung Cancer 45(1):19–27

3. Hammerschlag G, Cao J, Gumm K, Irving L, Steinfort D(2015) Prevalence of incidental pulmonary nodules on com-puted tomography of the thorax in trauma patients. InternMed J 45(6):630–633

4. Momen M. Wahidi, Joseph A. Govert, Ranjit K. Goudar, et al.Evidence for the Treatment of Patients With Pulmonary Nodules:When Is It Lung Cancer? ACCP Evidence-Based Clinical PracticeGuidelines (2nd Edition)

5. Manhire A, Charig M, Clelland C, Gleeson F, Miller R, Moss H,Pointon K, Richardson C (2003) Sawicka E; BTS. Guidelines forradiologically guided lung biopsy. Thorax 58(11):920–936

6. Laroche C, Fairbairn I, Moss H, Pepke-Zaba J, Sharples L, FlowerC, Coulden R (2000) Role of computed tomographic scanning ofthe thorax prior to bronchoscopy in the investigation of suspectedlung cancer. Thorax 55(5):359–363

7. Collins CD, Breatnach E, Nath PH (1992) Percutaneous needlebiopsy of lung nodules following failed bronchoscopic biopsy.Eur J Radiol 15(1):49–53

8. Goldsmith SJ, Kostakoglu L (2000) Role of nuclear medicine in theevaluation of the solitary pulmonary nodule. Semin Ultrasound CTMR 21(2):129–138

9. Gould MK, Maclean CC, Kuschner WG, Rydzak CE, Owens DKAccuracy of positron emission tomography for diagnosis of pulmo-nary nodules and mass lesions: a meta-analysis. JAMA2001;21;285(7):914–24

10. Erasmus JJ, McAdams HP, Connolly JE (2000) Solitary pulmonarynodules: part II. Evaluation of the indeterminate nodule.Radiographics 20(1):59–66

11. Erasmus JJ, McAdams HP, Patz EF Jr, Coleman RE, Ahuja V,Goodman PC (1998) Evaluation of primary pulmonary carcinoidtumors using FDG PET. AJR Am J Roentgenol 170(5):1369–1373

12. Higashi K, Ueda Y, Seki H, Yuasa K, Oguchi M, Noguchi T,Taniguchi M, Tonami H, Okimura T, Yamamoto I (1998)

Fluorine-18-FDG PET imaging is negative in bronchioloalveolarlung carcinoma. J Nucl Med 39(6):1016–1020

13. MacMahon H, Austin JH, Gamsu G, Herold CJ, Jett JR,Naidich DP, Patz EF Jr (2005) Swensen SJ; FleischnerSociety. Guidelines for management of small pulmonarynodules detected on CT scans: a statement from theFleischner Society. Radiology 237(2):395–400

14. Gruden JF, Klein SJ, Webb WR (1993) Percutaneous trans-thoracic needle biopsy in AIDS: analysis in 32 patients.Radiology 189:567–571

15. Sinner WN (1984) Fine needle biopsy of tuberculomas. Chest 85:836

16. Hoffer FA, Gow K, Flynn PM et al (2001) Accuracy of percutane-ous lung biopsy for invasive pulmonary aspergillosis. Pediat Radiol31:144–152

17. Nosari A, Anghilieri M, Carrafiello G, Guffanti C et al (2003)Utility of percutaneous lung biopsy for diagnosing filamentous fun-gal infections in hematologic malignancies. Haematologica 88(12):1405–1409

18. Carrafiello G, Laganà D, Nosari AM, Guffanti C et al (2006) Utilityof computed tomography (CT) and of fine needle aspiration biopsy(FNAB) in early diagnosis of fungal pulmonary infections. Study ofinfections from filamentous fungi in haematologically immunode-ficient patients. Radiol Med 111(1):33–41

19. Raptakis T, Boura P, Tsimpoukis S, Gkiozos I, Syrigos KN (2013)Endoscopic and endobronchial ultrasound-guided needle aspirationin the mediastinal staging of non-small cell lung cancer. AnticancerRes 33(6):2369–2376

20. Lange TJ, Kunzendorf F, Pfeifer M, Arzt M, Schulz C (2012)Endobronchial ultrasound-guided transbronchial needle aspirationin routine care - plenty of benign results and follow-up tests. Int JClin Pract 66(5):438–445

21. Carter BW, Marom EM, Detterbeck FC (2014) Approaching thepatient with an anterior mediastinal mass: a guide for clinicians. JThorac Oncol 9(9 Suppl 2):S102–S109

22. Carter BW, Okumura M, Detterbeck FC, Marom EM (2014)Approaching the patient with an anterior mediastinal mass: a guidefor radiologists. J Thorac Oncol 9(9 Suppl 2):S110–S118

23. Chouaid C, Dujon C, Monnet I, Madroszyk A, Le Caer H et al(2014) Feasibility and clinical impact of re-biopsy in advanced nonsmall-cell lung cancer: a prospective multicenter study in a real-world setting (GFPC study 12-01). Lung Cancer 86(2):170–173

24. Patel IJ, Davidson JC et al (2012) Consensus guidelines forperiprocedural management of coagulation status and hemostasisrisk in percutaneous image-guided interventions. J Vasc IntervRadiol 23(6):727–736

25. Laurent F, Montaudon M, Latrabe V, Bégueret H (2003)Percutaneous biopsy in lung cancer. Eur J Radiol 45(1):60–68

26. Klein JS, Zarka MA (1997) Transthoracic needle biopsy: an over-view. J Thorac Imaging 12(4):232–249

27. Sheth S, Harper UH, Stanley DB et al (1999) US guidance forthoracic biopsy: a valuable alternative to CT. Radiology 210(3):721–726

28. Winokur RS, Pua BB, Sullivan BW, Madoff DC (2013)Percutaneous lung biopsy: technique, efficacy, and complications.Semin Intervent Radiol. 30(2):121–127

29. Anzidei M, Argirò R, Porfiri A, Boni F et al (2015) Preliminaryclinical experience with a dedicated interventional robotic systemfor CT-guided biopsies of lung lesions: a comparison with the con-ventional manual technique. Eur Radiol 25(5):1310–1316

30. Romanes GJ (1981) Cunningham’s textbook of anatomy. OxfordUniversity Press, London

31. Glassberg RM, Sussman SK, Glickstein MF (1990) CTanatomy ofthe internal mammary vessels: importance in planning percutane-ous transthoracic procedures. AJR 155:397–400

Insights Imaging (2017) 8:419–428 427

32. Yankelevitz DF, Vazquez M, Henschke CI (2000) Special tech-niques in transthoracic needle biopsy of pulmonary nodules.Radiol Clin N Am 38:267–279

33. Lang EK, Ghavami R, Schreiner VC, Archibald S, Ramirez J(2000) Autologous blood clot seal to prevent pneumothorax atCT-guided lung biopsy. Radiology 216(1):93–96

34. Wagner JM, Hinshaw JL (2011) LubnerMG, et al. CT-guided lungbiopsies: pleural blood patching reduces the rate of chest tube place-ment for postbiopsy pneumothorax. AJR Am J Roentgenol 197(4):783–788

35. DiBardino DM, Yarmus LB, Semaan RW (2015) Transthoracicneedle biopsy of the lung. J Thorac Dis 7(Suppl 4):S304–S316

36. Capalbo E, Peli M, Lovisatti M, Cosentino M et al (2014) Trans-thoracic biopsy of lung lesions: FNAB or CNB? Our experienceand review of the literature. Radiol Med 119(8):572–594

37. Schneider F, Smith MA, Lane MC et al (2015) Adequacy of coreneedle biopsy specimens and fine-needle aspirates for moleculartesting of lung adenocarcinomas. Am J Clin Pathol 143(2):193–200 quiz 306

38. Layfield LJ, Coogan A, Johnston WW et al (1996) Transthoracicfine needle aspiration biopsy. Sensitivity in relation to guidancetechnique and lesion size and location. Acta Cytol 40:687–690

39. Yamagami T, Kato T, Iida S et al (2004) Percutaneous needle biopsyfor small lung nodules beneath the rib under CT scan fluoroscopicguidance with gantry tilt. Chest 126:744–747

40. Wang Y, Jiang F, Tan X, Tian P (2016) CT-guided percutaneoustransthoracic needle biopsy for paramediast inal andnonparamediastinal lung lesions: diagnostic yield and complica-tions in 1484 patients. Medicine 95(31):e4460

41. Wu CC, Maher MM, Shepard JA (2011 Jun) Complications of CT-guided percutaneous needle biopsy of the chest: prevention andmanagement. AJR Am J Roentgenol 196(6):W678–W682

42. AnzideiM, Sacconi B, Fraioli F, Saba L et al (2015) Development ofa prediction model and risk score for procedure-related complica-tions in patients undergoing percutaneous computed tomography-guided lung biopsy. Eur J Cardiothorac Surg 48(1):e1–e6

43. Birchard KR (2011) Transthoracic needle biopsy. Semin InterventRadiol 28:87–97

44. Traill ZC, Gleeson FV (1997) Delayed pneumothorax after CT-guided percutaneous fine needle aspiration lung biopsy. Thorax52:581–582

45. Wu CC, Maher MM, Shepard JA (2011) Complications of CT-guided percutaneous needle biopsy of the chest: prevention andmanagement. AJR Am J Roentgenol 196:W678–W682

46. Geraghty PR, Kee ST, McFarlane G et al (2003) CT-guided trans-thoracic needle aspiration biopsy of pulmonary nodules: needle sizeand pneumothorax rate. Radiology 229:475–481

47. CollingsCL WJL, BansonNL LRC (1999) Pneumothorax and de-pendent versus nondependent patient position after needle biopsy ofthe lung. Radiology 210(1):59–64

48. Heck SL, Blom P, Berstad A (2006) Accuracy and complications incomputed tomography fluoroscopy-guided needle biopsies of lungmasses. Eur Radiol 16(6):1387–1392

49. Cox JE, Chiles C, McManus CM, Aquino SL, Choplin RH (1999)Transthoracic needle aspiration biopsy: variables that affect risk ofpneumothorax. Radiology 212(1):165–168

50. Kazerooni EA, Lim FT, Mikhail A, Martinez FJ (1996) Risk ofpneumothorax in CT-guided transthoracic needle aspiration biopsyof the lung. Radiology 198(2):371–375

51. Ko JP, Shepard JO, Drucker EA et al (2001) Factors influencingpneumothorax rate at lung biopsy: are dwell time and angle ofpleural puncture contributing factors? Radiology 218(2):491–496

52. Khankan AA, Al-Muaikeel M (2012) Image-guided percutaneoustransthoracic biopsy in lung cancer emphasis on CT-guided tech-nique. J Infect Public Health 5(Suppl 1):S22–S30

53. YamagamiT NT, Iida S, Kato T, Nishimura T (2002) Managementof pneumothorax after percutaneous CT-guided lung biopsy. Chest121(4):1159–1164

54. Henry M, Arnold T, Harvey J (2003) BTS guidelines for the man-agement of spontaneous pneumothorax. In: BTS guidelines for themanagement of pleural disease. Thorax 58(Suppl II):ii39–ii52

55. Sinner WN (1976) Complications of percutaneous transthoracicneedle aspiration biopsy. Acta Radiol Diagn (Stockh) 17(6):813–828

56. Berquist TH, Bailey PB, Cortese DA et al (1980) Transthoracicneedle biopsy: accuracy and complications in relation to locationand type of lesion. Mayo Clin Proc 55:475–481

57. Tai R, Dunne R, Trotman-Dickenson B, Jacobson F et al (2016)Frequency and severity of pulmonary hemorrhage in patients un-dergoing percutaneous CT-guided transthoracic lung biopsy:single-institution experience of 1175 cases. Radiology 279(1):287–296

58. Milner LB, Ryan K, Gullo J (1979) Fatal intratho- racic hemorrhageafter percutaneous aspiration lung biopsy. AJR Am J Roentgenol132(2):280–281

59. Khankan A, Sirhan S, Aris F (2015) Common complications ofnonvascular percutaneous thoracic interventions: diagnosis andmanagement. Semin Intervent Radiol 32(2):174–181

60. Freund MC, Petersen J, Goder KC, Bunse T, Wiedermann F,Glodny B (2012) Systemic air embolism during percutaneous coreneedle biopsy of the lung: frequency and risk factors. BMC PulmMed 12:2

61. Tomiyama N, Yasuhara Y, Nakajima Y, Adachi S et al (2006) CT-guided needle biopsy of lung lesions: a survey of severe complica-tion based on 9783 biopsies in Japan. Eur J Radiol 59(1):60–64

62. Hare SS, Gupta A, Goncalves AT, Souza CA, Matzinger F, SeelyJM (2011) Systemic arterial air embolism after percutaneous lungbiopsy. Clin Radiol 66(7):589–596

63. Voravud N, ShinDM,Dekmezian RH, Dimery I, Lee JS, HongWK(1992) Implantation metastasis of carcinoma after percutaneousfine-needle aspiration biopsy. Chest 102(1):313–315

64. Agarwal PP, Seely JM, Matzinger FR, MacRae RM, Peterson RA,Maziak DE, Dennie CJ (2006) Pleural mesothelioma: sensitivityand incidence of needle track seeding after image-guided biopsyversus surgical biopsy. Radiology 241(2):589–594

65. Kim GR, Hur J, Lee SM et al (2011) CT fluoroscopy-guided lungbiopsy versus conventional CT-guided lung biopsy: a prospectivecontrolled study to assess radiation doses and diagnostic perfor-mance. Eur Radiol

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